11
views
0
recommends
+1 Recommend
0 collections
    0
    shares
      • Record: found
      • Abstract: found
      • Article: found
      Is Open Access

      Collective information storage in multiple synapses enables fast learning and slow forgetting

      abstract
      1 , , 1 , 2 , 3
      BMC Neuroscience
      BioMed Central
      24th Annual Computational Neuroscience Meeting: CNS*2015
      18-23 July 2015

      Read this article at

      Bookmark
          There is no author summary for this article yet. Authors can add summaries to their articles on ScienceOpen to make them more accessible to a non-specialist audience.

          Abstract

          Most of the excitatory cortical synapses reside on dendritic spines. Although these spines undergo a remarkably high turnover [1,2], they have been shown to be involved in learning and long-term memory. Along this line, it is unclear how information is preserved while its substrate (synapses or spines) is permanently changing. Here, we use a simple stochastic model of structural plasticity to investigate this phenomenon : We assume a certain number of potential synaptic locations from one neuron to another. At those locations, synapses (spines) are created with a constant probability and removed with a probability depending on the number of existing synapses and the stimulation of the neurons. From these two probabilities, the stationary distribution of the number of synapses between two neurons can be calculated. Experimental measurements of these stationary probability distributions in the cortex show that the majority of connections has either zero or multiple synapses while one or two contacts are very improbable [e.g., [3-5]]. Using information theoretic measures we show that, in our model, such bimodal distributions enable information storage over time scales many orders of magnitudes higher than the involved probabilities. Thus, in this system the conflict of rapid spine turnover (probabilities) and long-term memory is resolved by storing the information collaboratively in multiple synapses. In the following, we will consider the bimodal stationary distributions as the working point of the system. Then, we can model external signals, as, e.g., increased or decreased activities during learning, as changes of the removal probabilities and stationary distributions (e.g., mediated by synaptic plasticity [6]). For instance, for learning signals resulting to unimodal stationary distributions (only connected or only unconnected), we find that learning is orders of magnitude faster than forgetting. Along this line, we observe that retraining a task does not induce an increased overturn rate as during initial training, which has been similarly observed for dendritic spines in vivo [1,2]. Our results clearly relate the difference in time scales to the shape of the stationary distribution and therefore reveal the functional advantage of the bimodal distribution found in experiment.

          Related collections

          Most cited references4

          • Record: found
          • Abstract: found
          • Article: not found

          Synaptic connections between layer 4 spiny neurone-layer 2/3 pyramidal cell pairs in juvenile rat barrel cortex: physiology and anatomy of interlaminar signalling within a cortical column.

          Whole-cell voltage recordings were obtained from 64 synaptically coupled excitatory layer 4 (L4) spiny neurones and L2/3 pyramidal cells in acute slices of the somatosensory cortex ('barrel' cortex) of 17- to 23-days-old rats. Single action potentials (APs) in the L4 spiny neurone evoked single unitary EPSPs in the L2/3 pyramidal cell with a peak amplitude of 0.7 +/- 0.6 mV. The average latency was 2.1 +/- 0.6 ms, the rise time was 0.8 +/- 0.3 ms and the decay time constant was 12.7 +/- 3.5 ms. The percentage of failures of an AP in a L4 spiny neurone to evoke a unitary EPSP in the L2/3 pyramidal cell was 4.9 +/- 8.8 % and the coefficient of variation (c.v.) of the unitary EPSP amplitude was 0.27 +/- 0.13. Both c.v. and percentage of failures decreased with increased average EPSP amplitude. Postsynaptic glutamate receptors (GluRs) in L2/3 pyramidal cells were of the N-methyl-D-aspartate (NMDA) receptor (NMDAR) and the non-NMDAR type. At -60 mV in the presence of extracellular Mg2+ (1 mM), 29 +/- 15 % of the EPSP voltage-time integral was blocked by NMDAR antagonists. In 0 Mg2+, the NMDAR/AMPAR ratio of the EPSC was 0.50 +/- 0.29, about half the value obtained for L4 spiny neurone connections. Burst stimulation of L4 spiny neurones showed that EPSPs in L2/3 pyramidal cells depressed over a wide range of frequencies (1-100 s(-1) ). However, at higher frequencies (30 s(-1)) EPSP summation overcame synaptic depression so that the summed EPSP was larger than the first EPSP amplitude in the train. The number of putative synaptic contacts established by the axonal collaterals of the L4 projection neurone with the target neurone in layer 2/3 varied between 4 and 5, with an average of 4.5 +/- 0.5 (n = 13 pairs). Synapses were established on basal dendrites of the pyramidal cell. Their mean geometric distance from the pyramidal cell soma was 67 +/- 34 microm (range, 16-196 microm). The results suggest that each connected L4 spiny neurone produces a weak but reliable EPSP in the pyramidal cell. Therefore transmission of signals to layer 2/3 is likely to have a high threshold requiring simultaneous activation of many L4 neurons, implying that L4 spiny neurone to L2/3 pyramidal cell synapses act as a gate for the lateral spread of excitation in layer 2/3.
            Bookmark
            • Record: found
            • Abstract: found
            • Article: not found

            Reliable synaptic connections between pairs of excitatory layer 4 neurones within a single 'barrel' of developing rat somatosensory cortex.

            1. Dual whole-cell recordings were made from pairs of synaptically coupled excitatory neurones in the 'barrel field' in layer (L) 4 in slices of young (postnatal day 12-15) rat somatosensory cortex. The majority of interconnected excitatory neurones were spiny stellate cells with an asymmetrical dendritic arborisation largely confined to a single barrel. The remainder were star pyramidal cells with a prominent apical dendrite terminating in L2/3 without forming a tuft. 2. Excitatory synaptic connections were examined between 131 pairs of spiny L4 neurones. Single presynaptic action potentials evoked unitary EPSPs with a peak amplitude of 1.59 +/- 1.51 mV (mean +/- s. d.), a latency of 0.92 +/- 0.35 ms, a rise time of 1.53 +/- 0.46 ms and a decay time constant of 17.8 +/- 6.3 ms. 3. At 34-36 C, the coefficient of variation (c.v.) of the unitary EPSP amplitude was 0. 37 +/- 0.16 and the percentage of failures to evoke an EPSP was 5.3 +/- 7.8 %. The c.v. and failure rate decreased with increasing amplitude of the unitary EPSP. 4. Postsynaptic glutamate receptors in spiny L4 neurones were of the AMPA and NMDA type. At -60 mV in the presence of 1 mM Mg2+, NMDA receptors contributed 39.3 +/- 12.5 % to the EPSP integral. In Mg2+-free solution, the NMDA receptor/AMPA receptor ratio of the EPSC was 0.86 +/- 0.64. 5. The number of putative synaptic contacts established by the projection neurone with the target neurone varied between two and five with a mean of 3.4 +/- 1.0 (n = 11). Synaptic contacts were exclusively found in the barrel in which the cell pair was located and were preferentially located on secondary to quarternary dendritic branches. Their mean geometric distance from the soma was 68.8 +/- 37.4 microm (range, 33.4-168.0 microm). The number of synaptic contacts and mean EPSP amplitude showed no significant correlation. 6. The results suggest that in L4 of the barrel cortex synaptic transmission between spiny neurones is largely restricted to a single barrel. The connections are very reliable, probably due to a high release probability, and have a high efficacy because of the compact structure of the dendrites and axons of spiny neurones. Intrabarrel connections thus function to amplify and distribute the afferent thalamic activity in the vertical directions of a cortical column.
              Bookmark
              • Record: found
              • Abstract: found
              • Article: not found

              Presynaptic efficacy directs normalization of synaptic strength in layer 2/3 rat neocortex after paired activity.

              Paired neuronal activity is known to induce changes in synaptic strength that result in the synapse in question having different properties to unmodified synapses. Here we show that in layer 2/3 excitatory connections in young adult rat cortex paired activity acts to normalize the strength and quantal parameters of connections. Paired action potential firing produces long-term potentiation in only a third of connections, whereas a third remain with their amplitude unchanged and a third exhibit long-term depression. Furthermore, the direction of plasticity can be predicted by the initial strength of the connection: weak connections potentiate and strong connections depress. A quantal analysis reveals that changes in synaptic efficacy were predominantly presynaptic in locus and that the key determinant of the direction and magnitude of synaptic modification was the initial release probability (P(r)) of the synapse, which correlated inversely with change in P(r) after pairing. Furthermore, distal synapses also exhibited larger potentiations including postsynaptic increases in efficacy, whereas more proximal inputs did not. This may represent a means by which distal synapses preferentially increase their efficacy to achieve equal weighting at the soma. Paired activity thus acts to normalize synaptic strength, by both pre- and postsynaptic mechanisms.
                Bookmark

                Author and article information

                Contributors
                Conference
                BMC Neurosci
                BMC Neurosci
                BMC Neuroscience
                BioMed Central
                1471-2202
                2015
                4 December 2015
                : 16
                : Suppl 1
                : O15
                Affiliations
                [1 ]Bernstein Center for Computaional Neuroscience, Third Physics Institute, Göttingen, Germany
                [2 ]Max Planck Institute for Dynamics and Self-Organization, Göttingen, Germany
                [3 ]Weizman Institute, Rehovot, Israel
                Article
                1471-2202-16-S1-O15
                10.1186/1471-2202-16-S1-O15
                4697653
                41ca4828-69ec-47c3-b5ab-a6677909e9e3
                Copyright © 2015 Fauth et al.

                This is an Open Access article distributed under the terms of the Creative Commons Attribution License ( http://creativecommons.org/licenses/by/4.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited. The Creative Commons Public Domain Dedication waiver ( http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.

                24th Annual Computational Neuroscience Meeting: CNS*2015
                Prague, Czech Republic
                18-23 July 2015
                History
                Categories
                Oral Presentation

                Neurosciences
                Neurosciences

                Comments

                Comment on this article